Characterization of Escherichia coli bloodstream isolates associated with mortality

Journal of Medical Microbiology

Volumn 65, Issue 1, 2016, Pages 71-79

  Miajlovic, Helen ^a   Aogáin, Micheál Mac ^a   Collins, Cathal J ^a,c   Rogers, Thomas R ^a,b   Smith, Stephen G J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b ST JAMES S HOSPITAL   (Ireland)

^c CAVAN GENERAL HOSPITAL   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; BACTERIAL DNA; BACTERIAL TOXIN; VIRULENCE FACTOR; ANTIINFECTIVE AGENT; CULTURE MEDIUM;

ADULT; AGED; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM CULTURE; BACTERIUM ISOLATE; BLOODSTREAM INFECTION; CLINICAL ARTICLE; DNA EXTRACTION; ESCHERICHIA COLI INFECTION; FEMALE; GENE SEQUENCE; HUMAN; IMMUNE EVASION; MALE; MIDDLE AGED; MORTALITY; MULTIDRUG RESISTANCE; NEUTROPHIL; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; VERY ELDERLY; BACTEREMIA; BACTERIUM IDENTIFICATION; BLOOD; CLASSIFICATION; CULTURE MEDIUM; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; GENETICS; IRELAND; ISOLATION AND PURIFICATION; MULTILOCUS SEQUENCE TYPING;

ADULT; AGED; AGED, 80 AND OVER; ANTI-BACTERIAL AGENTS; BACTEREMIA; BACTERIAL TYPING TECHNIQUES; CULTURE MEDIA; DNA, BACTERIAL; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FEMALE; HUMANS; IRELAND; MALE; MIDDLE AGED; MULTILOCUS SEQUENCE TYPING;

EID: 84957599598     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.000200     Document Type: Article

References (61)

1. Alhashash, F., Weston, V., Diggle, M. & McNally, A. (2013). Multidrug-resistant Escherichia coli bacteremia. Emerg Infect Dis 19, 1699–1701.
2. Alqasim, A., Emes, R., Clark, G., Newcombe, J., La Ragione, R. & McNally, A. (2014). Phenotypic microarrays suggest Escherichia coli ST131 is not a metabolically distinct lineage of extra-intestinal pathogenic E. coli. PLoS One 9, e88374.
3. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. (1990). Basic local alignment search tool. J Mol Biol 215, 403–410.
4. Antão, E. M., Wieler, L. H. & Ewers, C. (2009). Adhesive threads of extraintestinal pathogenic Escherichia coli. Gut Pathog 1, 22.
5. Bankevich, A., Nurk, S., Antipov, D., Gurevich, A. A., Dvorkin, M., Kulikov, A. S., Lesin, V. M., Nikolenko, S. I., Pham, S. & other authors (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19, 455–477.
6. Bolger, A. M., Lohse, M. & Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120.
7. Buckles, E. L., Wang, X., Lane, M. C., Lockatell, C. V., Johnson, D. E., Rasko, D. A., Mobley, H. L. & Donnenberg, M. S. (2009). Role of the K2 capsule in Escherichia coli urinary tract infection and serum resistance. J Infect Dis 199, 1689–1697.
8. Bullen, J. J., Rogers, H. J., Spalding, P. B. & Ward, C. G. (2005). Iron and infection: the heart of the matter. FEMS Immunol Med Microbiol 43, 325–330.
9. Cirl, C., Wieser, A., Yadav, M., Duerr, S., Schubert, S., Fischer, H., Stappert, D., Wantia, N., Rodriguez, N. & other authors (2008). Subversion of Toll-like receptor signaling by a unique family of bacterial Toll/interleukin-1 receptor domain-containing proteins. Nat Med 14, 399–406.
10. CLSI (2015). Performance Standards for Antimicrobial Susceptibility Testing; Approved Standard, 12th edn. Supplement M100-S22. Wayne, PA: Clinical and Laboratory Standards Institute.
11. Coque, T. M., Novais, A., Carattoli, A., Poirel, L., Pitout, J., Peixe, L., Baquero, F., Cantón, R. & Nordmann, P. (2008). Dissemination of clonally related Escherichia coli strains expressing extended-spectrum b-lactamase CTX-M-15. Emerg Infect Dis 14, 195–200.
12. Dahbi, G., Mora, A., Mamani, R., López, C., Alonso, M. P., Marzoa, J., Blanco, M., Herrera, A., Viso, S. & other authors (2014). Molecular epidemiology and virulence of Escherichia coli O16: H5-ST131: comparison with H30 and H30-Rx subclones of O25b: H4-ST131. Int J Med Microbiol 304, 1247–1257.
13. de Kraker, M. E., Jarlier, V., Monen, J. C., Heuer, O. E., van de Sande, N. & Grundmann, H. (2013). The changing epidemiology of bacteraemias in Europe: trends from the European Antimicrobial Resistance Surveillance System. Clin Microbiol Infect 19, 860–868.
14. Dobrindt, U., Agerer, F., Michaelis, K., Janka, A., Buchrieser, C., Samuelson, M., Svanborg, C., Gottschalk, G., Karch, H. & Hacker, J. (2003). Analysis of genome plasticity in pathogenic and commensal Escherichia coli isolates by use of DNA arrays. J Bacteriol 185, 1831–1840.
15. Fagan, R. P. & Smith, S. G. (2007). The Hek outer membrane protein of Escherichia coli is an auto-aggregating adhesin and invasin. FEMS Microbiol Lett 269, 248–255.
16. Gibreel, T. M., Dodgson, A. R., Cheesbrough, J., Bolton, F. J., Fox, A. J. & Upton, M. (2012a). High metabolic potential may contribute to the success of ST131 uropathogenic Escherichia coli. J Clin Microbiol 50, 3202–3207.
17. Gibreel, T. M., Dodgson, A. R., Cheesbrough, J., Fox, A. J., Bolton, F. J. & Upton, M. (2012b). Population structure, virulence potential and antibiotic susceptibility of uropathogenic Escherichia coli from northwest England. J Antimicrob Chemother 67, 346–356.
18. Hekker, T. A., Groeneveld, A. B., Simoons-Smit, A. M., de Man, P., Connell, H. & MacLaren, D. M. (2000). Role of bacterial virulence factors and host factors in the outcome of Escherichia coli bacteraemia. Eur J Clin Microbiol Infect Dis 19, 312–316.
19. Henderson, J. P., Crowley, J. R., Pinkner, J. S., Walker, J. N., Tsukayama, P., Stamm, W. E., Hooton, T. M. & Hultgren, S. J. (2009). Quantitative metabolomics reveals an epigenetic blueprint for iron acquisition in uropathogenic Escherichia coli. PLoS Pathog 5, e1000305.
20. Homann, C., Varming, K., Høgåsen, K., Mollnes, T. E., Graudal, N., Thomsen, A. C. & Garred, P. (1997). Acquired C3 deficiency in patients with alcoholic cirrhosis predisposes to infection and increased mortality. Gut 40, 544–549.
21. Horner, C., Fawley, W., Morris, K., Parnell, P., Denton, M. & Wilcox, M. (2014). Escherichia coli bacteraemia: 2 years of prospective regional surveillance (2010-12). J Antimicrob Chemother 69, 91–100.
22. Hui, C. Y., Guo, Y., He, Q. S., Peng, L., Wu, S. C., Cao, H. & Huang, S. H. (2010). Escherichia coli outer membrane protease OmpT confers resistance to urinary cationic peptides. Microbiol Immunol 54, 452–459.
23. Jauréguy, F., Carbonnelle, E., Bonacorsi, S., Clec’h, C., Casassus, P., Bingen, E., Picard, B., Nassif, X. & Lortholary, O. (2007). Host and bacterial determinants of initial severity and outcome of Escherichia coli sepsis. Clin Microbiol Infect 13, 854–862.
24. Johnson, J. R. (1991). Virulence factors in Escherichia coli urinary tract infection. Clin Microbiol Rev 4, 80–128.
25. Johnson, J. R., Menard, M., Johnston, B., Kuskowski, M. A., Nichol, K. & Zhanel, G. G. (2009). Epidemic clonal groups of Escherichia coli as a cause of antimicrobial-resistant urinary tract infections in Canada, 2002 to 2004. Antimicrob Agents Chemother 53, 2733–2739.
26. Johnson, J. R., Johnston, B., Clabots, C., Kuskowski, M. A. & Castanheira, M. (2010). Escherichia coli sequence type ST131 as the major cause of serious multidrug-resistant E. coli infections in the United States. Clin Infect Dis 51, 286–294.
27. Jolley, K. A. & Maiden, M. C. (2010). BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11, 595.
28. Kaper, J. B., Nataro, J. P. & Mobley, H. L. (2004). Pathogenic Escherichia coli. Nat Rev Microbiol 2, 123–140.
29. Köhler, C. D. & Dobrindt, U. (2011). What defines extraintestinal pathogenic Escherichia coli? Int J Med Microbiol 301, 642–647.
30. Laupland, K. B., Gregson, D. B., Church, D. L., Ross, T. & Pitout, J. D. (2008). Incidence, risk factors and outcomes of Escherichia coli bloodstream infections in a large Canadian region. Clin Microbiol Infect 14, 1041–1047.
31. Lefort, A., Panhard, X., Clermont, O., Woerther, P. L., Branger, C., Mentré, F., Fantin, B., Wolff, M., Denamur, E. & COLIBAFI Group (2011). Host factors and portal of entry outweigh bacterial determinants to predict the severity of Escherichia coli bacteremia. J Clin Microbiol 49, 777–783.
32. Lodinová-Žádniková, R. & Sonnenborn, U. (1997). Effect of preventive administration of a nonpathogenic Escherichia coli strain on the colonization of the intestine with microbial pathogens in newborn infants. Biol Neonate 71, 224–232.
33. Miajlovic, H. & Smith, S. G. (2014). Bacterial self-defence: how Escherichia coli evades serum killing. FEMS Microbiol Lett 354, 1–9.
34. Miajlovic, H., Cooke, N. M., Moran, G. P., Rogers, T. R. & Smith, S. G. (2014). Response of extraintestinal pathogenic Escherichia coli to human serum reveals a protective role for Rcs-regulated exopolysaccharide colanic acid. Infect Immun 82, 298–305.
35. Miles, A. A., Misra, S. S. & Irwin, J. O. (1938). The estimation of the bactericidal power of the blood. J Hyg (Lond) 38, 732–749.
36. Mills, M., Meysick, K. C. & O’Brien, A. D. (2000). Cytotoxic necrotizing factor type 1 of uropathogenic Escherichia coli kills cultured human uroepithelial 5637 cells by an apoptotic mechanism. Infect Immun 68, 5869–5880.
37. Mobley, H. L., Green, D. M., Trifillis, A. L., Johnson, D. E., Chippendale, G. R., Lockatell, C. V., Jones, B. D. & Warren, J. W. (1990). Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains. Infect Immun 58, 1281–1289.
38. Mulvey, M. A., Schilling, J. D., Martinez, J. J. & Hultgren, S. J. (2000). Bad bugs and beleaguered bladders: interplay between uropathogenic Escherichia coli and innate host defenses. Proc Natl Acad Sci U S A 97, 8829–8835.
39. Nicolas-Chanoine, M. H., Blanco, J., Leflon-Guibout, V., Demarty, R., Alonso, M. P., Caniça, M. M., Park, Y. J., Lavigne, J. P., Pitout, J. & Johnson, J. R. (2008). Intercontinental emergence of Escherichia coli clone O25: H4-ST131 producing CTX-M-15. J Antimicrob Chemother 61, 273–281.
40. Nicolas-Chanoine, M. H., Bertrand, X. & Madec, J. Y. (2014). Escherichia coli ST131, an intriguing clonal group. Clin Microbiol Rev 27, 543–574.
41. Nipicˇ, D., Podlesek, Z., Budicˇ, M., Cˇ rnigoj, M. & Žgur-Bertok, D. (2013). Escherichia coli uropathogenic-specific protein, Usp, is a bacteriocin-like genotoxin. J Infect Dis 208, 1545–1552.
42. Oh, H., Siano, B. & Diamond, S. (2008). Neutrophil isolation protocol. J Vis Exp 17, 745.
43. Ortega, M., Marco, F., Soriano, A., Almela, M., Martínez, J. A., Muñoz, A. & Mensa, J. (2009). Analysis of 4758 Escherichia coli bacteraemia episodes: predictive factors for isolation of an antibiotic-resistant strain and their impact on the outcome. J Antimicrob Chemother 63, 568–574.
44. Peralta, G., Roiz, M. P., Sánchez, M. B., Garrido, J. C., Ceballos, B., Rodríguez-Lera, M. J., Mateos, F. & De Benito, I. (2007). Time-topositivity in patients with Escherichia coli bacteraemia. Clin Microbiol Infect 13, 1077–1082.
45. Phan, M.-D., Peters, K. M., Sarkar, S., Lukowski, S. W., Allsopp, L. P., Gomes Moriel, D. G., Achard, M. E. S., Totsika, M., Marshall, V. M. & other authors (2013). The serum resistome of a globally disseminated multidrug resistant uropathogenic Escherichia coli clone. PLoS Genet 9, e1003834.
46. Pitout, J. D., Laupland, K. B., Church, D. L., Menard, M. L. & Johnson, J. R. (2005). Virulence factors of Escherichia coli isolates that produce CTX-M-type extended-spectrum b-lactamases. Antimicrob Agents Chemother 49, 4667–4670.
47. Qin, X. & Gao, B. (2006). The complement system in liver diseases. Cell Mol Immunol 3, 333–340.
48. Russo, T. A. & Johnson, J. R. (2003). Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly important endemic problem. Microbes Infect 5, 449–456.
49. Sarma, J. V. & Ward, P. A. (2011). The complement system. Cell Tissue Res 343, 227–235.
50. Skaar, E. P. (2010). The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathog 6, e1000949.
51. Skjøt-Rasmussen, L., Ejrnæs, K., Lundgren, B., Hammerum, A. M. & Frimodt-Møller, N. (2012). Virulence factors and phylogenetic grouping of Escherichia coli isolates from patients with bacteraemia of urinary tract origin relate to sex and hospital- vs. communityacquired origin. Int J Med Microbiol 302, 129–134.
52. Smith, Y. C., Rasmussen, S. B., Grande, K. K., Conran, R. M. & O’Brien, A. D. (2008). Hemolysin of uropathogenic Escherichia coli evokes extensive shedding of the uroepithelium and hemorrhage in bladder tissue within the first 24 hours after intraurethral inoculation of mice. Infect Immun 76, 2978–2990.
53. Smith, S. N., Hagan, E. C., Lane, M. C. & Mobley, H. L. (2010). Dissemination and systemic colonization of uropathogenic Escherichia coli in a murine model of bacteremia. MBio 1, e00262–e00210.
54. Subashchandrabose, S., Smith, S. N., Spurbeck, R. R., Kole, M. M. & Mobley, H. L. (2013). Genome-wide detection of fitness genes in uropathogenic Escherichia coli during systemic infection. PLoS Pathog 9, e1003788.
55. Ulett, G. C., Valle, J., Beloin, C., Sherlock, O., Ghigo, J. M. & Schembri, M. A. (2007). Functional analysis of antigen 43 in uropathogenic Escherichia coli reveals a role in long-term persistence in the urinary tract. Infect Immun 75, 3233–3244.
56. Ulett, G. C., Totsika, M., Schaale, K., Carey, A. J., Sweet, M. J. & Schembri, M. A. (2013). Uropathogenic Escherichia coli virulence and innate immune responses during urinary tract infection. Curr Opin Microbiol 16, 100–107.
57. Vimont, S., Boyd, A., Bleibtreu, A., Bens, M., Goujon, J. M., Garry, L., Clermont, O., Denamur, E., Arlet, G. & Vandewalle, A. (2012). The CTX-M-15-producing Escherichia coli clone O25b: H4-ST131 has high intestine colonization and urinary tract infection abilities. PLoS One 7, e46547.
58. Watts, R. E., Totsika, M., Challinor, V. L., Mabbett, A. N., Ulett, G. C., De Voss, J. J. & Schembri, M. A. (2012). Contribution of siderophore systems to growth and urinary tract colonization of asymptomatic bacteriuria Escherichia coli. Infect Immun 80, 333–344.
59. Weissman, S. J., Johnson, J. R., Tchesnokova, V., Billig, M., Dykhuizen, D., Riddell, K., Rogers, P., Qin, X., Butler-Wu, S. & other authors (2012). High-resolution two-locus clonal typing of extraintestinal pathogenic Escherichia coli. Appl Environ Microbiol 78, 1353–1360.
60. Wirth, T., Falush, D., Lan, R., Colles, F., Mensa, P., Wieler, L. H., Karch, H., Reeves, P. R., Maiden, M. C. & other authors (2006). Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60, 1136–1151.
61. Wurpel, D. J., Totsika, M., Allsopp, L. P., Hartley-Tassell, L. E., Day, C. J., Peters, K. M., Sarkar, S., Ulett, G. C., Yang, J. & other authors (2014). F9 fimbriae of uropathogenic Escherichia coli are expressed at low temperature and recognise Galb1-3GlcNAccontaining glycans. PLoS One 9, e93177.